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July 1991 - October 2014
Education
September 1977 - October 1983
September 1973 - January 1977
Publications
Publications (432)
Highly sensitive in situ hybridization procedures (RNAScope) were used to quantify the expression of three dopamine receptors (Drd1, Drd2, and Drd3) in two song control nuclei (HVC and the Area X of the basal ganglia) that are known to receive dopaminergic inputs and in the periaqueductal gray (PAG) of male and female canaries. Both sexes were trea...
The auditory sensitivity of a small songbird, the red-cheeked cordon bleu, was measured using the standard methods of animal psychophysics. Hearing in cordon bleus is similar to other small passerines with best hearing in the frequency region from 2 to 4 kHz and sensitivity declining at the rate of about 10 dB/octave below 2 kHz and about 35 dB/oct...
Birdsong is an excellent system for studying complex vocal signaling in both males and females. Historically, most research in captivity has focused only on male song. This has left a gap in our understanding of the environmental, neuroendocrine, and mechanistic control of female song. Here, we report the overall acoustic features, repertoire, and...
A species' success during the invasion of new areas hinges on an interplay between the demographic processes common to invasions and the specific ecological context of the novel environment. Evolutionary genetic studies of invasive species can investigate how genetic bottlenecks and ecological conditions shape genetic variation in invasions, and ou...
Social relationships, affiliative social attachments, are important for many species. The best studied types of relationships are monogamous pair bonds. However, it remains unclear how generalizable models of pair bonding are across types of social attachments. Zebra finches are a fascinating system to explore the neurobiology of social relationshi...
Background
Behavioral sex differences are widespread in the animal world. These differences can be qualitative (i.e., behavior present in one sex but not the other, a true sex dimorphism) or quantitative (behavior is present at a higher rate or quality in one sex compared to the other). Singing in oscine songbirds is associated with both types of d...
Birdsong is a relatively well-studied behavior, both due to its importance as a model for vocal production learning and as an intriguing complex social behavior. Until the last few decades, work on birdsong focused almost exclusively on males. However, it is now widely accepted that female song not only exists, but is fairly common throughout the o...
We previously confirmed that effects of testosterone (T) on singing activity and on the volume of brain song control nuclei are sexually differentiated in adult canaries: females are limited in their ability to respond to T as males do. Here we expand on these results by focusing on sex differences in the production and performance of trills, i.e.,...
The song control nucleus HVC of songbirds has emerged as a widespread model system to study adult neurogenesis and the factors that modulate the incorporation of new neurons, including seasonal state, sex differences or sex steroid hormone concentrations. However, the specific function of these new neurons born in adulthood remains poorly understoo...
We previously confirmed that effects of testosterone (T) on singing activity and on the volume of brain song control nuclei are sexually differentiated in adult canaries: females are limited in their ability to respond to T as males do. Here we expand on these results by focusing on sex differences in the production and performance of trills, i.e.,...
Background. Behavioral sex differences are widespread in the animal world. These differences can be qualitative (i.e., behavior present in one sex but not the other, a true sex dimorphism) or quantitative (behavior is present at a higher rate or quality in one sex compared to the other). Singing in oscine songbirds is associated with both types of...
Recent psychophysical experiments have shown that zebra finches (Taeniopygia guttata-a songbird) are surprisingly insensitive to syllable sequence changes in their species-specific motifs while budgerigars (Melopsittacus undulatus-a psittacine) do much better when tested on exactly the same sounds. This is unexpected since zebra finch males learn t...
The song control nucleus HVC of songbirds has emerged as a widespread model system to study adult neurogenesis and the factors that modulate the incorporation of new neurons, including seasonal state, sex differences or sex steroid hormone concentrations. However, the specific function of these new neurons born in adulthood remains poorly understoo...
Birdsong is a relatively well-studied behavior, both due to its importance as a model for vocal production learning and as an intriguing complex social behavior. Until the last few decades work on birdsong focused almost exclusively on males. However, it is now widely accepted that female song not only exists, but is fairly common throughout the os...
Ronald (Ron) Barfield was born in Detroit Michigan on 25 July 1936 and devoted his entire career to the study of the endocrine control of behavior. His research was heavily influenced by the ethological tradition that he was exposed to through his PhD advisor Nicholas Collias. After postdoctoral studies at the Institute of Animal Behavior at Rutger...
Mei-Fang Cheng was a behavioral neuroendocrinologist who was born in Taiwan but pursued graduate and postdoctoral studies in the United States. She then joined the laboratory of Daniel Lehrman at the Institute of Animal Behavior, Rutgers University-Newark, where she spent her entire career first as a research associate and then in 1969 as an assist...
Jacques Balthazart is a Belgian behavioral neuroendocrinologist whose work focused on the neuroendocrineNeuroendocrine regulation of reproductive behaviorsBehaviors of birdsBirds, primarily based on studies in Japanese quailQuail and songbirds. He is best known for his studies of the organizational and activational actions of sex steroidsSex steroi...
Social cues modulate the neuroendocrine control of reproduction. However, the neural systems involved in the integration of social cues are not well described. Gonadotropin-releasing hormone 1 (GnRH1) cells in the preoptic area (POA) are the final common node that links the brain with peripheral reproductive physiology. These experiments investigat...
Temperate-zone birds display marked seasonal changes in reproductive behaviors and the underlying hormonal and neural mechanisms. These changes were extensively studied in canaries (Serinus canaria) but differ between strains. Fife fancy male canaries change their reproductive physiology in response to variations in day length but it remains unclea...
Adult treatments with testosterone (T) do not activate singing behavior nor promote growth of song control nuclei to the same extent in male and female canaries (Serinus canaria). Because T acts in part via aromatization into an estrogen and brain aromatase activity is lower in females than in males in many vertebrates, we hypothesized that this en...
Thyroid hormones clearly play a role in the seasonal regulation of reproduction, but any role they might play in song behavior and the associated seasonal neuroplasticity in songbirds remains to be elucidated. To pursue this question, we first established seasonal patterns in the expression of thyroid hormone regulating genes in male European starl...
Birdsong is controlled in part by a discrete network of interconnected brain nuclei regulated in turn by steroid hormones and environmental stimuli. This complex interaction results in neural changes that occur seasonally as the environment varies (e.g., photoperiod, food/water availability, etc.). Variation in environment, vocal behavior, and neur...
The European starling, Sturnus vulgaris, is an ecologically significant, globally invasive avian species that is also suffering from a major decline in its native range. Here, we present the genome assembly and long‐read transcriptome of an Australian‐sourced European starling (S. vulgaris vAU), and a second, North American, short‐read genome assem...
The avian homologue of oxytocin (OT), formerly called mesotocin, influences social behaviors in songbirds and potentially song production. We sought to characterize the distribution of OT peptide in the brain of two songbird species: canaries (Serinus canaria) and zebra finches (Taeniopygia guttata). To visualize OT, we performed immunocytochemistr...
Male song in songbirds is a critical and elaborate signal for mate attraction. In many species female listeners respond to male song both behaviorally and physiologically (e.g. copulation solicitation displays and production of the immediate early gene ZENK in auditory regions). It is becoming increasingly well known that females in many species al...
In male Japanese quail, brain aromatase is crucial for the hormonal activation of sexual behavior, but the sites producing neuro‐estrogens critical for these behaviors have not been completely identified. This study examined the function of aromatase expressed in several nuclei of the social behavior network on a measure of sexual motivation known...
This chapter presents in a synthetic manner, the wealth of information that has accumulated primarly in the past 50–60 years concerning the mechanisms through which hormones modulate behaviors. It provides an introduction on how hormones are able to affect brain activity in relation to the control of behaviour, and describes the major concepts that...
Classically, estrogens regulate male sexual behavior through effects initiated in the nucleus. However, neuroestrogens, i.e., estrogens locally produced in the brain, can act within minutes via membrane-initiated events. In male quail, rapid changes in brain aromatase activity occur after exposure to sexual stimuli. We report here that local extrac...
Birdsong has been the subject of broad research from a variety of sub-disciplines and has taught us much about the evolution, function, and mechanisms driving animal communication and cognition. Typically, birdsong refers to the specialized vocalizations produced by oscines. Historically, much of the research on birdsong was conducted in north temp...
Songbirds learn their vocalizations during developmental sensitive periods of song memorization and sensorimotor learning. Some seasonal songbirds, called open-ended learners, recapitulate transitions from sensorimotor learning and song crystallization on a seasonal basis during adulthood. In adult male canaries, sensorimotor learning occurs each y...
A new study employing viral targeting techniques has identified excitatory and inhibitory cell groups in the songbird auditory forebrain that exhibit properties remarkably similar to those in the mammalian cortex. This network contributes to the neural substrate mediating sophisticated cognition in birds.
A species' success during the invasion of new areas hinges on an interplay between demographic processes and the outcome of localized selection. Invasive European Starlings (Sturnus vulgaris) established populations in Australia and North America in the 19th century. Here, we compare whole-genome sequences among native and independently introduced...
Songbirds learn their vocalizations during sensitive periods of song memorization and sensorimotor learning during development. Some seasonal songbirds, called open-ended learners, recapitulate transitions from sensorimotor learning and song crystallization on a seasonal basis during adulthood. In adult male canaries, sensorimotor learning occurs e...
Numerous studies have evaluated changes in time of testicular development in birds by exploratory laparotomy or post-mortem autopsy. The invasive nature of these approaches has obviously limited the frequency at which these measures can be collected. We demonstrate here that accurate assessment of gonadal size can be reliably and repeatedly obtaine...
Aromatase converts androgens into estrogens in the brain of vertebrates including humans. This enzyme is also expressed in other tissues where its action may result in negative effects on human health (e.g., promotion of tumor growth). To prevent these effects, aromatase inhibitors were developed and are currently used to block human estrogen-depen...
The European starling, Sturnus vulgaris, is an ecologically significant, globally invasive avian species that is also suffering from a major decline in its native range. Here, we present the genome assembly and long-read transcriptome of an Australian-sourced European starling (S. vulgaris vAU), and a second North American genome (S. vulgaris vNA),...
Studies of acoustic communication often focus on the categories and units of vocalizations, but subtle variation also occurs in how these signals are uttered. In human speech, it is not only phonemes and words that carry information but also the timbre, intonation, and stress of how speech sounds are delivered (often referred to as “paralinguistic...
Research on monogamy has largely focused on marked behaviors that are unique to pair bonded partners. However, these marked behaviors represent only a subset of the pair-directed behaviors that partners engage in; the influence of pair bonding on mundane or subtle social interactions among partners remains largely unknown. In the current study, we...
Male canaries (Serinus canaria) display seasonal changes in the motivation to sing which have been found to be dependent on the action of testosterone (T). During the breeding season when T is high, males sing at a higher rate compared with males with low T. The effect of T on song rate is known to be mediated by the medial preoptic nucleus (POM);...
In the 1970s, Nottebohm and Arnold reported marked male-biased sex differences in the volume of three song control nuclei in songbirds. Subsequently a series of studies on several songbird species suggested that there is a positive correlation between the degree to which there is a sex difference in the volume of these song control nuclei and in so...
Research on monogamy has largely focused on marked behaviors that are unique to pair bonded partners. However, these marked behaviors represent only a subset of the pair-directed behaviors that partners engage in; the influence of pair bonding on mundane or subtle social interactions among partners remains largely unknown. In the current study, we...
Testosterone aromatization into estrogens in the preoptic area (POA) is critical for the activation of male sexual behavior in many vertebrates. Yet, cellular mechanisms mediating actions of neuroestrogens on sexual behavior remain largely unknown. We investigated in male and female Japanese quail by dual‐label fluorescent in situ hybridization (FI...
Songbirds are a powerful model to study vocal learning given that aspects of the underlying behavioral and neurobiological mechanisms are analogous in many ways to mechanisms involved in speech learning. Perineuronal nets (PNNs) represent one of the mechanisms controlling the closing of sensitive periods for vocal learning in the songbird brain. In...
Songbirds learn their song during a sensitive period of development associated with enhanced neural plasticity. In addition, in open-ended learners such as canaries, a sensitive period for sensorimotor vocal learning reopens each year in the fall and leads to song modifications between successive breeding seasons. The variability observed in song p...
Perineuronal nets (PNN) of the extracellular matrix are dense aggregations of chondroitin-sulfate proteoglycans that usually surround fast-spiking parvalbumin-expressing inhibitory interneurons (PV). The development of PNN around PV appears specifically at the end of sensitive periods of visual learning and limits the synaptic plasticity in the vis...
The complex and melodic nature of many birds' songs has raised interest in potential parallels between avian vocal sequences and human speech. The similarities between birdsong and speech in production and learning are well established, but surprisingly little is known about how birds perceive song sequences. One popular laboratory songbird, the ze...
An individual's ability to respond to and align with the behavior of others is a fundamental component of social behavior. Zebra finches form lifelong monogamous pair bonds; however, zebra finches are also gregarious and can form strong social bonds with same-sex conspecifics. Here, we quantified behavior during brief 10-min reunions for males and...
Temperate zone songbird species, such as the canary (Serinus canaria), can serve as model systems to investigate adult seasonal plasticity in brain and behavior. An increase in day length, experienced by canaries in the early spring stimulates gonadal recrudescence and an associated increase in circulating testosterone concentrations. This increase...
Almost fifty years ago the advent of assay methods to measure circulating levels of hormones revolutionized endocrinology in relation to investigations of free-living and captive animals. This new field "environmental endocrinology" revealed that endocrine profiles in animals in their natural habitat were not only different from captive animals, bu...
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ABSTRACT
Breeders have bred canaries either for specific song characteristics (song canaries) or morphology/plumage (type canaries) for centuries. Type canaries (e.g., Border and Gloster strains) retain song characteristics that are typically quite similar to those of wild canaries. By contrast, song canaries (e.g., Belgian Watersl...
In male songbirds, song functions to attract a mate or to defend a territory; it is therefore often produced in the context of reproduction. Testosterone of gonadal origin increases during the reproductive phase of the annual cycle and significantly enhances song production as well as song development via effects on song crystallization. The neural...
The authors of the original challenge hypothesis proposed influential hypotheses concerning the relationship between testosterone concentrations in the blood and aggressive social behaviors. Many of the key observations were made in avian species studied in the wild and in captivity. In this review we evaluate some remaining questions about the ide...
Belgian Waterslager song canaries, bred for hundreds of years for a low-pitched song, have also acquired an inherited high-frequency hearing loss associated with hair cell abnormalities. Here, auditory thresholds measured using auditory brainstem responses and psychophysical methods in three different strains of canaries are compared: Belgian Water...
In male songbirds, the motivation to sing is largely regulated by testosterone (T) action in the medial preoptic area, whereas T acts on song control nuclei to modulate aspects of song quality. Stereotaxic implantation of T in the medial preoptic nucleus (POM) of castrated male canaries activates a high rate of singing activity, albeit with a longe...
Aromatization within the medial preoptic nucleus (POM) is essential for the expression of male copulatory behavior in Japanese quail. However, several nuclei within the social behavior network (SBN) also express aromatase. Whether aromatase in these loci participates in the behavioral activation is not known. Castrated male Japanese quail were impl...
Testosterone activates singing within days in castrated male songbirds but full song quality only develops after a few weeks. Lesions of the medial preoptic nucleus (POM) inhibit while stereotaxic testosterone implants into this nucleus increase singing rate suggesting that this site plays a key role in the regulation of singing motivation. Testost...
The melodic, rolling songs of canaries have entertained humans for centuries and have been studied for decades by researchers interested in vocal learning, but relatively little is known about how the birds listen to their songs. Here, it is investigated how discriminable the general acoustic features of conspecific songs are to canaries, and their...
This study was designed to determine whether changes in sexual motivation acutely regulate brain estrogen synthesis by aromatase. Five experiments (Exp.1–5) were first conducted to determine the effect of recent mating and of the presentation of a new female (Coolidge effect) on sexual motivation. Exp.1–2 showed that 10 min or overnight access to c...
There is a rich history of behavioral and neurobiological research focused on the ‘syntax’ of birdsong as a model for human language and complex auditory perception. Zebra finches are one of the most widely studied songbird species in this area of investigation. As they produce song syllables in a fixed sequence, it is reasonable to assume that adu...
In seasonally breeding songbirds such as canaries, singing behavior is predominantly under the control of testosterone and its metabolites. Short daylenths in the fall that break photorefractoriness are followed by increasing daylengths in spring that activate singing via both photoperiodic and hormonal mechanisms. However, we observed in a group o...
The ability to discriminate changes in the fine structure of complex sounds is well developed in birds. However, the precise limit of this discrimination ability and how it is used in the context of natural communication remains unclear. Here we describe natural variability in acoustic fine structure of male and female zebra finch calls. Results fr...
Sex steroid hormones act during early development to shape the circuitry upon which these same hormones act in adulthood to control behavioral responses to various stimuli. The "organizational" vs. "activational" distinction was proposed to explain this temporal difference in hormone action. In both of these cases steroids were thought to act genom...
Budgerigars, a small species of parrot, are open-ended vocal learners that produce a long, rambling warble song. Past work has shown that these birds are sensitive to changes in the order of their song elements but it is not clear what rules they may use to process changes in sounds sequences. Here, we used operant conditioning and psychophysical t...
The temporal fine structure (TFS) of an acoustic signal refers to the smaller changes within the time waveform, independent of larger envelope changes. Bioacousticians typically have relied on sonographic analyses to describe the primary acoustic features of animal vocalizations and human speech. However, sonographic analyses do not reveal the temp...
Estrogens exert pleiotropic effects on multiple physiological and behavioral traits including sexual behavior. These effects are classically mediated via binding to nuclear receptors and subsequent regulation of target gene transcription. Estrogens also affect neuronal activity and cell-signaling pathways via faster, membrane-initiated events. Alth...
In male quail, estrogens produced in the brain (neuroestrogens) exert a dual action on male sexual behavior: they increase sexual motivation within minutes via mechanisms activated at the membrane but facilitate sexual performance by slower, presumably nuclear-initiated, mechanisms. Recent work indicates that neuroestrogens are also implicated in t...
The neural basis of how learned vocalizations change during development and in adulthood represents a major challenge facing cognitive neuroscience. This plasticity in the degree to which learned vocalizations can change in both humans and songbirds is linked to the actions of sex steroid hormones during ontogeny but also in adulthood in the contex...
Previous work has shown that birds. in general, and zebra finches. in particular, have remarkable sensitivity to temporal fine structure (TFS). While spectral, envelope, and TFS cues are present in vocalizations, TFS has been largely ignored since sonographic, and not time waveform, analyses have been the mainstay in bioacoustics. However, birds’ i...
Zebra finches have become a popular model for the investigation of the motor and perceptual mechanisms underlying vocal learning. These birds are closed-ended learners that have a brief sensitive period for song learning, after which a new song cannot be learned. This song is a single, highly stereotyped, invariant, sequence of 3-8 harmonic syllabl...
Canaries have become important models for the study of vocal learning. The male produces long song bouts up to a minute long consisting of various syllables, each repeated in flexibly sequenced phrases. Little is known about how the birds listen to song though behavioral observations clearly show that female canaries are more sexually responsive to...
Mate separation has been shown to mediate changes in physiological and behavioral processes via activation of the hypothalamo‐pituitary‐adrenal (HPA) axis in both mammalian and avian species. In order to elucidate the neural mechanisms associated with changes in the HPA axis in response to social stress, we investigated the effects of mate pair sep...
This chapter will focus on how brain and behavior can change with season. Given the breadth of the topic, we will focus on prominent examples discerned from studies of birds though other vertebrate species will be discussed. The chapter will begin with a general discussion of the environmental control of seasonal changes in brain and behavior. We w...
Perineuronal nets (PNN) are aggregations of chondroitin sulfate proteoglycans surrounding the soma and proximal processes of neurons, mostly GABAergic interneurons expressing parvalbumin. They limit the plasticity of their afferent synaptic connections. In zebra finches PNN develop in an experience-dependent manner in the song control nuclei HVC an...
Estrogens are known to act rapidly, probably via membrane estrogen receptors, to induce fast effects on physiological and behavioral processes. Engaging in some of these behaviors, such as sexual behavior, results in an acute modulation of the production of estrogens in the brain by regulating the efficiency of the estrogen synthase enzyme, aromata...
In songbirds, neurogenesis in the song control nucleus HVC is sensitive to the hormonal and social environment but the dynamics of this process is difficult to assess with a single exogenous marker of new neurons. We simultaneously used three independent markers to investigate HVC neurogenesis in male and female canaries. Males were castrated, impl...
Final full data set.
(XLSX)
Testosterone plays a key role in the control of seasonal changes in singing behavior and its underlying neural circuitry. After administration of exogenous testosterone, song quality and song control nuclei volumes change over the course of weeks, but song rate increases within days. The medial preoptic nucleus (POM) controls sexual motivation and...